Multiple striatal representation in primate substantia nigra.

The pattern of arborization of the striatonigral fibers in the squirrel monkey (Saimiri sciureus) was studied with Phaseolus vulgaris-leucoagglutinin (PHA-L) and biocytin as anterograde tracers. Single, small injections of PHA-L or biocytin in either the caudate nucleus or the putamen give rise to at least four distinct, nonoverlapping but interconnected fiber plexuses that are distributed throughout the rostrocaudal extent of the substantia nigra pars reticulata (SNr) according to a strikingly precise and constant sequence. These plexuses, which comprise numerous fibers that closely entwine unlabeled dendrites of SNr neurons (woolly fibers), often lie at the base of dopaminergic cell columns of the substantia nigra pars compacta (SNc). Long and varicose fibers emerge dorsally from SNr plexuses and climb along the ventrally oriented dendrites of dopaminergic SNc neurons, as visualized with tyrosine hydroxylase immunohistochemistry. These fibers appear to contact en passant both dendrites and cell bodies of dopaminergic neurons belonging to the ventral tier of SNc. Anterograde double-labeling experiments involving small deposits of PHA-L and biocytin in adjacent areas of the caudate nucleus and the putamen reveal that neighboring striatonigral cell populations form two distinct sets of terminal plexuses that remain well segregated throughout SNr. Plexuses from the two sources interdigitate in some parts of SNr, but never intermix. Furthermore, the woolly fibers in these plexuses are composed exclusively of either PHA-L- or biocytin-labeled elements; none of them display both types of labeling. These results reveal that the striatonigral projection in primates is highly divergent and that the striatum has multiple representations at nigral levels. They also indicate that striatal information is conveyed to the substantia nigra in a highly ordered fashion through multiple segregated channels.